scholarly journals Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

2020 ◽  
Author(s):  
Meetali Singh ◽  
Eric Cornes ◽  
Blaise Li ◽  
Piergiuseppe Quarato ◽  
Loan Bourdon ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Rna Polymerase ◽  
Codon Usage ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Coding Sequences ◽  
Germ Granules ◽  
Rna Biogenesis

In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with ribosome translation in the cytoplasm, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

scholarly journals Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

2020 ◽  
Author(s):  
Germano Cecere ◽  
Meetali Singh ◽  
Eric Cornes ◽  
Blaise Li ◽  
Piergiuseppe Quarato ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Rna Polymerase ◽  
Codon Usage ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Coding Sequences ◽  
Germ Granules ◽  
Rna Biogenesis

Abstract In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with ribosome translation in the cytoplasm, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

scholarly journals Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Meetali Singh ◽  
Eric Cornes ◽  
Blaise Li ◽  
Piergiuseppe Quarato ◽  
Loan Bourdon ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Rna Polymerase ◽  
Codon Usage ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Coding Sequences ◽  
Germ Granules ◽  
Rna Biogenesis

AbstractIn the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with translating ribosomes, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

scholarly journals The Caenorhabditis elegans TDRD5/7-like protein, LOTR-1, interacts with the helicase ZNFX-1 to balance epigenetic signals in the germline

2021 ◽  
Author(s):  
Elisabeth A Marnik ◽  
Miguel Vasconcelos Almeida ◽  
P Giselle Cipriani ◽  
George Chung ◽  
Edoardo Caspani ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Small Rna ◽  
Small Rnas ◽  
Brood Size ◽  
Homologous Proteins ◽  
P Granules ◽  
Transposon Silencing ◽  
Tudor Domain ◽  
Germ Granules

LOTUS and Tudor domain containing proteins have critical roles in the germline. Proteins that contain these domains, such as Tejas/Tapas in Drosophila, help localize Vasa to the germ granules and facilitate piRNA-mediated transposon silencing. The homologous proteins in mammals, TDRD5 and TDRD7, are required during spermiogenesis. Until now, proteins containing both LOTUS and Tudor domains in Caenorhabditis elegans have remained elusive. Here we describe LOTR-1 (D1081.7), which derives its name from its LOTUS and Tudor domains. Interestingly, LOTR-1 docks next to P granules to colocalize with the broadly conserved Z-granule helicase, ZNFX-1. LOTR-1's Z-granule association requires its Tudor domain, but both LOTUS and Tudor deletions affect brood size when coupled with a knockdown of the Vasa homolog glh-1. In addition to interacting with the germ-granule components WAGO-1, PRG-1 and DEPS-1, we identified a Tudor-dependent association with ZNFX-1. Like znfx-1 mutants, lotr-1 mutants lose small RNAs from the 3' ends of WAGO and Mutator targets, reminiscent of the loss of piRNAs from the 3' ends of piRNA precursor transcripts in mouse Tdrd5 mutants. Our work suggests that LOTR-1 acts in a conserved mechanism that brings small RNA generating mechanisms towards the 3' ends of small RNA templates or precursors.

scholarly journals The IDR-containing protein PID-2 affects Z granules and is required for piRNA-induced silencing in the embryo

2020 ◽  
Author(s):  
Maria Placentino ◽  
António Miguel de Jesus Domingues ◽  
Jan Schreier ◽  
Sabrina Dietz ◽  
Svenja Hellmann ◽  
...  
Keyword(s):  
Gene Regulation ◽  
Caenorhabditis Elegans ◽  
Rna Polymerase ◽  
Small Rna ◽  
Rna Silencing ◽  
Rna Dependent Rna Polymerase ◽  
Prolyl Aminopeptidase ◽  
C Elegans

AbstractIn Caenorhabditis elegans, the piRNA (21U RNA) pathway is required to establish proper gene regulation and an immortal germline. To achieve this, PRG-1-bound 21U RNAs trigger silencing mechanisms mediated by RNA-dependent RNA polymerase (RdRP)-synthetized 22G RNAs. This silencing can become PRG-1-independent, and heritable over many generations. This state is named RNAe. It is unknown how and when RNAe is established, and how it is maintained. We show that maternally provided 21U RNAs can be sufficient to trigger RNAe in embryos. Additionally, we identify the IDR-containing protein PID-2, as a factor required to establish and maintain RNAe. PID-2 interacts with two novel, partially redundant, eTudor domain proteins, PID-4 and PID-5. Additionally, PID-5 has a domain related to the X-prolyl aminopeptidase protein APP-1, and binds APP-1, implicating N-terminal proteolysis in RNAe. All three proteins are required for germline immortality, localize to perinuclear foci, affect Z granules, and are required for balancing of 22G RNA populations. Overall, our study identifies three new proteins with crucial functions in the C. elegans small RNA silencing network.

scholarly journals GTSF-1 is required for the formation of a functional RNA-dependent RNA Polymerase complex in C. elegans

2018 ◽  
Author(s):  
Miguel Vasconcelos Almeida ◽  
Sabrina Dietz ◽  
Stefan Redl ◽  
Emil Karaulanov ◽  
Andrea Hildebrandt ◽  
...  
Keyword(s):  
Rna Polymerase ◽  
Gene Silencing ◽  
Small Rna ◽  
Small Rnas ◽  
Zinc Fingers ◽  
Specific Factor ◽  
Rna Dependent Rna Polymerase ◽  
C Elegans ◽  
Argonaute Proteins ◽  
Rna Pathways

AbstractIn every domain of life, Argonaute proteins and their associated small RNAs regulate gene expression. Despite great conservation of Argonaute proteins throughout evolution, many proteins acting in small RNA pathways are not widely conserved. Gametocyte-specific factor 1 (Gtsf1) proteins, characterized by two tandem CHHC zinc fingers and an unstructured, acidic C-terminal tail, are conserved in animals and act in small RNA pathways. In fly and mouse, they are required for fertility and have been shown to interact with Piwi clade Argonautes. We identified T06A10.3 as the Caenorhabditis elegans Gtsf1 homolog and named it gtsf-1. Given its conserved nature and roles in Piwi-mediated gene silencing, we sought out to characterize GTSF-1 in the context of the small RNA pathways of C. elegans. Like its homologs, GTSF-1 is required for normal fertility. Surprisingly, we report that GTSF-1 is not required for Piwi-mediated gene silencing. Instead, gtsf-1 mutants show strong depletion of a class of endogenous small RNAs, known as 26G-RNAs, and fully phenocopy mutants lacking RRF-3, the RNA-dependent RNA Polymerase that synthesizes 26G-RNAs. We show, both in vivo and in vitro, that GTSF-1 specifically and robustly interacts with RRF-3 via its tandem CHHC zinc fingers. Furthermore, we demonstrate that GTSF-1 is required for the assembly of a larger RRF-3 and DCR-1-containing complex, also known as ERIC, thereby allowing for 26G-RNA generation. We propose that GTSF-1 homologs may similarly act to drive the assembly of larger complexes that subsequently act in small RNA production and/or in imposing small RNA-mediated silencing activities.

scholarly journals Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development

2012 ◽  
pp. no-no ◽  
Author(s):  
Xianwei Song ◽  
Dekai Wang ◽  
Lijia Ma ◽  
Zhiyu Chen ◽  
Pingchuan Li ◽  
...  
Keyword(s):  
Rna Polymerase ◽  
Small Rna ◽  
Rna Dependent Rna Polymerase ◽  
Rna Biogenesis

scholarly journals Intertissue small RNA communication mediates the acquisition and inheritance of hormesis in Caenorhabditis elegans

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Emiko Okabe ◽  
Masaharu Uno ◽  
Saya Kishimoto ◽  
Eisuke Nishida
Keyword(s):  
Caenorhabditis Elegans ◽  
Small Rna ◽  
Stress Resistance ◽  
Environmental Conditions ◽  
Production System ◽  
Small Rnas ◽  
Communication Systems ◽  
Rna Transport ◽  
Phenotypic Changes ◽  
Induced Stress

AbstractEnvironmental conditions can cause phenotypic changes, part of which can be inherited by subsequent generations via soma-to-germline communication. However, the signaling molecules or pathways that mediate intertissue communication remain unclear. Here, we show that intertissue small RNA communication systems play a key role in the acquisition and inheritance of hormesis effects – stress-induced stress resistance – in Caenorhabditis elegans. The miRNA-processing enzyme DRSH-1 is involved in both the acquisition and the inheritance of hormesis, whereas worm-specific Argonaute (WAGO) proteins, which function with endo-siRNAs, are involved only in its inheritance. Further analyses demonstrate that the miRNA production system in the neuron and the small RNA transport machinery in the intestine are both essential for its acquisition and that both the transport of small RNAs in the germline and the germline Argonaute HRDE-1 complex are required for its inheritance. Our results thus demonstrate that overlapping and distinct roles of small RNA systems in the acquisition and inheritance of hormesis effects.

scholarly journals Intronic regions of plant genes potentially encode RDR (RNA-dependent RNA polymerase)-dependent small RNAs

2015 ◽  
Vol 66 (7) ◽  
pp. 1763-1768 ◽  
Author(s):  
Jingping Qin ◽  
Xiaoxia Ma ◽  
Zili Yi ◽  
Yijun Meng ◽  
Zhonghai Tang
Keyword(s):  
Rna Polymerase ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Double Stranded Rna ◽  
Plant Genes ◽  
Dependent Pathway

The opinion is put forward here that certain intronic regions of plant genes could be converted to double-stranded RNA precursors for sRNA production through an RDR-dependent pathway.

scholarly journals Analysis of RDR1/RDR2/RDR6-independent small RNAs in Arabidopsis thaliana improves MIRNA annotations and reveals novel siRNA loci

2017 ◽  
Author(s):  
Seth Polydore ◽  
Michael J. Axtell
Keyword(s):  
Gene Expression ◽  
Arabidopsis Thaliana ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Seq ◽  
Triple Mutant ◽  
Physiological Mechanisms ◽  
Protein Coding ◽  
Regulate Gene Expression ◽  
Rna Biogenesis

SummaryPlant small RNAs regulate key physiological mechanisms through post-transcriptional and transcriptional silencing of gene expression. sRNAs fall into two major categories: those that are reliant on RNA Dependent RNA Polymerases (RDRs) for biogenesis and those that aren’t. Known RDR-dependent sRNAs include phased and repeat-associated short interfering RNAs, while known RDR-independent sRNAs are primarily microRNAs and other hairpin-derived sRNAs. In this study, we produced and analyzed small RNA-seq libraries from rdr1/rdr2/rdr6 triple mutant plants. Only a small fraction of all sRNA loci were RDR1/RDR2/RDR6-independent; most of these were microRNA loci or associated with predicted hairpin precursors. We found 58 previously annotated microRNA loci that were reliant on RDR1, −2, or −6 function, casting doubt on their classification. We also found 38 RDR1/2/6-independent small RNA loci that are not MIRNAs or otherwise hairpin-derived, and did not fit into other known paradigms for small RNA biogenesis. These 38 small RNA-producing loci have novel biogenesis mechanisms, and are frequently located in the vicinity of protein-coding genes. Altogether, our analysis suggest that these 38 loci represent one or more new types of small RNAs in Arabidopsis thaliana.Significance StatementSmall RNAs regulate gene expression in plants and are produced through a variety of previously-described mechanisms. Here, we examine a set of previously undiscovered small RNA-producing loci that are produced by novel mechanisms.

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